Impact of light on leaf initiation: a matter of photosynthate availability in the apical bud?
Andreas Savvides A B C , Nikolaos Ntagkas A , Wim van Ieperen A , Janneke A. Dieleman B and Leo F. M. Marcelis A B
+ Author Affiliations
- Author Affiliations
A Horticultural Supply Chains, Wageningen University, PO Box 630, 6700AP Wageningen, The Netherlands.
B Wageningen UR Greenhouse Horticulture, PO Box 644, 6700AP Wageningen, The Netherlands.
C Corresponding author. Email: andreas.savvides@wur.nl
Functional Plant Biology 41(5) 547-556 https://doi.org/10.1071/FP13217
Submitted: 24 July 2013 Accepted: 16 December 2013 Published: 29 January 2014
Abstract
Radiation substantially affects leaf initiation rate (LIR), a key variable for plant growth, by influencing the heat budget and therefore the temperature of the shoot apical meristem. The photosynthetically active component of solar radiation (photosynthetic photon flux density; PPFD) is critical for plant growth and when at shade to moderate levels may also influence LIR via limited photosynthate availability. Cucumber and tomato plants were subjected to different PPFDs (2.5–13.2 mol m–2 day–1) and then LIR, carbohydrate content and diel net CO2 uptake of the apical bud were quantified. LIR showed saturating response to increasing PPFD in both species. In this PPFD range, LIR was reduced by 20% in cucumber and by 40% in tomato plants. Carbohydrate content and dark respiration were substantially reduced at low PPFD. LIR may be considered as an adaptive trait of plants to low light levels, which is likely to be determined by the local photosynthate availability. In tomato and cucumber plants, LIR can be markedly reduced at low PPFD in plant production systems at high latitudes, suggesting that models solely based on thermal time may not precisely predict LIR at low PPFD.
Additional keywords: cucumber (Cucumis sativus L.), leaf appearance, leaf unfolding, light intensity, shoot apical meristem, starch, sugars, tomato (Solanum lycopersicum L.).
References
Adams SR, Cockshull KE, Cave CRJ (2001) Effect of temperature on the growth and development of tomato fruits. Annals of Botany 88, 869–877.| Effect of temperature on the growth and development of tomato fruits.Crossref | GoogleScholarGoogle Scholar |
Beinhart G (1963) Effects of environment on meristematic development, leaf area, and growth of white clover. Crop Science 3, 209–213.
| Effects of environment on meristematic development, leaf area, and growth of white clover.Crossref | GoogleScholarGoogle Scholar |
Carabelli M, Possenti M, Sessa G, Ciolfi A, Sassi M, Morelli G, Ruberti I (2007) Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity. Genes & Development 21, 1863–1868.
| Canopy shade causes a rapid and transient arrest in leaf development through auxin-induced cytokinin oxidase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXps1alsr8%3D&md5=5158fb0afbd763a2eab9e168c7cb25a8CAS |
Chazdon RL, Fetcher N (1983) Light environments of tropical forests. In ‘Physiological ecology of plants of the wet tropics Vol. 12’. (Eds E Medina, HA Mooney, C Vázquez-Yánes) pp. 27–36. (Springer: Dordrecht, The Netherlands)
Chenu K, Franck N, Dauzat J, Barczi J, Rey H, Lecoeur J (2005) Integrated responses of rosette organogenesis, morphogenesis and architecture to reduced incident light in Arabidopsis thaliana results in higher efficiency of light interception. Functional Plant Biology 32, 1123–1134.
| Integrated responses of rosette organogenesis, morphogenesis and architecture to reduced incident light in Arabidopsis thaliana results in higher efficiency of light interception.Crossref | GoogleScholarGoogle Scholar |
Christophe A, Moulia B, Varlet-Grancher C (2006) Quantitative contributions of blue light and PAR to the photocontrol of plant morphogenesis in Trifolium repens (L.). Journal of Experimental Botany 57, 2379–2390.
| Quantitative contributions of blue light and PAR to the photocontrol of plant morphogenesis in Trifolium repens (L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnvF2lsr0%3D&md5=21cd2c4a5c91c18caa78629a0c098c33CAS | 16798853PubMed |
Clough B, Milthorpe F (1975) Effects of water deficit on leaf development in tobacco. Functional Plant Biology 2, 291–300.
Cookson SJ, Van Lijsebettens M, Granier C (2005) Correlation between leaf growth variables suggest intrinsic and early controls of leaf size in Arabidopsis thaliana. Plant, Cell & Environment 28, 1355–1366.
| Correlation between leaf growth variables suggest intrinsic and early controls of leaf size in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Dosio GAA, Rey H, Lecoeur J, Izquierdo NG, Aguirrezábal LAN, Tardieu F, Turc O (2003) A whole‐plant analysis of the dynamics of expansion of individual leaves of two sunflower hybrids. Journal of Experimental Botany 54, 2541–2552.
| A whole‐plant analysis of the dynamics of expansion of individual leaves of two sunflower hybrids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosVertb8%3D&md5=dc3157a1a24bc1e161c876826b04a7e4CAS |
Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. Journal of Experimental Botany 63, 3367–3377.
| Sugars, signalling, and plant development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotVSitbw%3D&md5=8bdc6090f5525c78efd198a4dc53ca88CAS | 22140246PubMed |
Farrar J, Pollock C, Gallagher J (2000) Sucrose and the integration of metabolism in vascular plants. Plant Science 154, 1–11.
| Sucrose and the integration of metabolism in vascular plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhvV2mt7g%3D&md5=ff17eb6120f191b6ad28411d537b4878CAS | 10725553PubMed |
Fleming AJ, McQueen-Mason S, Mandel T, Kuhlemeier C (1997) Induction of leaf primordia by the cell wall protein expansin. Science 276, 1415–1418.
| Induction of leaf primordia by the cell wall protein expansin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsFOjs70%3D&md5=8dd7a09c7f121394eb10104568e45a0dCAS |
Franklin KA, Whitelam GC (2005) Phytochromes and shade-avoidance responses in plants. Annals of Botany 96, 169–175.
| Phytochromes and shade-avoidance responses in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXps1ymtrw%3D&md5=afee8a32acd49df13e168e7d2b154d0dCAS | 15894550PubMed |
Freixes S, Thibaud MC, Tardieu F, Muller B (2002) Root elongation and branching is related to local hexose concentration in Arabidopsis thaliana seedlings. Plant, Cell & Environment 25, 1357–1366.
| Root elongation and branching is related to local hexose concentration in Arabidopsis thaliana seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotVCqsrk%3D&md5=829fc1cbe0bc88c4ddd363254aa2b63eCAS |
Geller GN, Smith WK (1982) Influence of leaf size, orientation, and arrangement on temperature and transpiration in three high-elevation, large-leafed herbs. Oecologia 53, 227–234.
| Influence of leaf size, orientation, and arrangement on temperature and transpiration in three high-elevation, large-leafed herbs.Crossref | GoogleScholarGoogle Scholar |
Givnish T (1988) Adaptation to sun and shade: a whole-plant perspective. Functional Plant Biology 15, 63–92.
Golz J (2006) Signalling between the shoot apical meristem and developing lateral organs. Plant Molecular Biology 60, 889–903.
| Signalling between the shoot apical meristem and developing lateral organs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkvFCqu7s%3D&md5=a6c45b715be6ccb81776956cab0fecf7CAS | 16724259PubMed |
Granier C, Tardieu F (1998) Is thermal time adequate for expressing the effects of temperature on sunflower leaf development? Plant, Cell & Environment 21, 695–703.
| Is thermal time adequate for expressing the effects of temperature on sunflower leaf development?Crossref | GoogleScholarGoogle Scholar |
Granier C, Massonnet C, Turc O, Muller B, Chenu K, Tardieu F (2002) Individual leaf development in Arabidopsis thaliana: a stable thermal-time-based programme. Annals of Botany 89, 595–604.
| Individual leaf development in Arabidopsis thaliana: a stable thermal-time-based programme.Crossref | GoogleScholarGoogle Scholar | 12099534PubMed |
Heuvelink E, Marcelis LFM (1996) Influence of assimilate supply on leaf formation in sweet pepper and tomato. Journal of Horticultural Science & Biotechnology 714, 405–414.
Ho LC (1988) Metabolism and compartmentation of imported sugars in sink organs in relation to sink strength. Annual Review of Plant Physiology and Plant Molecular Biology 39, 355–378.
| Metabolism and compartmentation of imported sugars in sink organs in relation to sink strength.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXltVOltrk%3D&md5=464f476767edada7c618869b1dc0fe0aCAS |
Hogewoning SW, Trouwborst G, Maljaars H, Poorter H, van Ieperen W, Harbinson J (2010) Blue light dose–responses of leaf photosynthesis, morphology, and chemical composition of Cucumis sativus grown under different combinations of red and blue light. Journal of Experimental Botany 61, 3107–3117.
| Blue light dose–responses of leaf photosynthesis, morphology, and chemical composition of Cucumis sativus grown under different combinations of red and blue light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVWktrY%3D&md5=27d3c4fb305049a0da2310c872ad0402CAS | 20504875PubMed |
Hussey G (1963a) Growth and development in the young tomato: I. The effect of temperature and light intensity on growth of the shoot apex and leaf primordia. Journal of Experimental Botany 14, 316–325.
| Growth and development in the young tomato: I. The effect of temperature and light intensity on growth of the shoot apex and leaf primordia.Crossref | GoogleScholarGoogle Scholar |
Hussey G (1963b) Growth and development in the young tomato: II. The effect of defoliation on the development of the shoot apex. Journal of Experimental Botany 14, 326–333.
| Growth and development in the young tomato: II. The effect of defoliation on the development of the shoot apex.Crossref | GoogleScholarGoogle Scholar |
Jamieson PD, Brooking IR, Porter JR, Wilson DR (1995) Prediction of leaf appearance in wheat: a question of temperature. Field Crops Research 41, 35–44.
| Prediction of leaf appearance in wheat: a question of temperature.Crossref | GoogleScholarGoogle Scholar |
Kerstetter RA, Poethig RS (1998) The specification of leaf identity during shoot development. Annual Review of Cell and Developmental Biology 14, 373–398.
| The specification of leaf identity during shoot development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnvFyisr8%3D&md5=2c7c1768eea259a17a3d6033bdf83952CAS | 9891788PubMed |
Kozuka T, Horiguchi G, Kim G-T, Ohgishi M, Sakai T, Tsukaya H (2005) The different growth responses of the Arabidopsis thaliana leaf blade and the petiole during shade avoidance are regulated by photoreceptors and sugar. Plant & Cell Physiology 46, 213–223.
| The different growth responses of the Arabidopsis thaliana leaf blade and the petiole during shade avoidance are regulated by photoreceptors and sugar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1eqtLY%3D&md5=1c8307a44eef138e213e4391aa697e76CAS |
Lafarge T, Tardieu F (2002) A model co-ordinating the elongation of all leaves of a sorghum cultivar was applied to both Mediterranean and Sahelian conditions. Journal of Experimental Botany 53, 715–725.
| A model co-ordinating the elongation of all leaves of a sorghum cultivar was applied to both Mediterranean and Sahelian conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlCks7c%3D&md5=4fdfcf1d8b949d354dc59d122cad76a6CAS | 11886892PubMed |
Marc J, Palmer JH (1976) Relationship between water potential and leaf and inflorescence initiation in Helianthus annuus. Physiologia Plantarum 36, 101–104.
| Relationship between water potential and leaf and inflorescence initiation in Helianthus annuus.Crossref | GoogleScholarGoogle Scholar |
Marcelis LFM (1993) Leaf formation in cucumber (Cucumis sativus L.) as influenced by fruit load, light and temperature. Gartenbauwissenschaft 58, 124–129.
Marcelis LFM (1994) A simulation model for dry matter partitioning in cucumber. Annals of Botany 74, 43–52.
Marcelis LFM, Gijzen H (1998) Evaluation under commercial conditions of a model of prediction of the yield and quality of cucumber fruits. Scientia Horticulturae 76, 171–181.
| Evaluation under commercial conditions of a model of prediction of the yield and quality of cucumber fruits.Crossref | GoogleScholarGoogle Scholar |
Moore B, Zhou L, Rolland F, Hall Q, Cheng W-H, Liu Y-X, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300, 332–336.
| Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXislyqtLY%3D&md5=5fa048ae6a7c5b499894d652c15d48afCAS | 12690200PubMed |
Newton P (1963) Studies on the expansion of the leaf surface: II. The influence of light intensity and daylength. Journal of Experimental Botany 14, 458–482.
| Studies on the expansion of the leaf surface: II. The influence of light intensity and daylength.Crossref | GoogleScholarGoogle Scholar |
Noguchi K (2005) Effects of light intensity and carbohydrate status on leaf and root respiration. In ‘Plant respiration. Vol. 18’. (Eds H Lambers, M Ribas-Carbo) pp. 63–83. (Springer: Dordrecht, The Netherlands)
Pantin F, Simonneau T, Rolland G, Dauzat M, Muller B (2011) Control of leaf expansion: a developmental switch from metabolics to hydraulics. Plant Physiology 156, 803–815.
| Control of leaf expansion: a developmental switch from metabolics to hydraulics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFWrtrs%3D&md5=566dd59ba0fa08c4f0823c59bfc9c7c2CAS | 21474437PubMed |
Pantin F, Simonneau T, Muller B (2012) Coming of leaf age: control of growth by hydraulics and metabolics during leaf ontogeny. New Phytologist 196, 349–366.
| Coming of leaf age: control of growth by hydraulics and metabolics during leaf ontogeny.Crossref | GoogleScholarGoogle Scholar | 22924516PubMed |
Pieters GA (1985) Effects of irradiation level on leaf growth of sunflower. Physiologia Plantarum 65, 263–268.
| Effects of irradiation level on leaf growth of sunflower.Crossref | GoogleScholarGoogle Scholar |
Poorter H, Fiorani F, Stitt M, Schurr U, Finck A, Gibon Y, Usadel B, Munns R, Atkin OK, Tardieu F, Pons TL (2012) The art of growing plants for experimental purposes: a practical guide for the plant biologist. Functional Plant Biology 39, 821–838.
| The art of growing plants for experimental purposes: a practical guide for the plant biologist.Crossref | GoogleScholarGoogle Scholar |
Sager JC, Smith WO, Edwards JL, Cyr KL (1988) Photosynthetic efficiency and phytochrome photoequilibria determination using spectral data. Transactions of the ASABE 31, 1882–1889.
Savvides A, Fanourakis D, van Ieperen W (2012) Co-ordination of hydraulic and stomatal conductances across light qualities in cucumber leaves. Journal of Experimental Botany 63, 1135–1143.
| Co-ordination of hydraulic and stomatal conductances across light qualities in cucumber leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1Ols7k%3D&md5=4cb8eacd59a27b679f8b0c7fb33cf36aCAS | 22121201PubMed |
Savvides A, van Ieperen W, Dieleman JA, Marcelis LFM (2013) Meristem temperature substantially deviates from air temperature even in moderate environments: is the magnitude of this deviation species-specific? Plant, Cell & Environment 36, 1950–1960.
Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant, Cell & Environment 30, 1126–1149.
| Coordination of carbon supply and plant growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVeiurrJ&md5=503bf3b7db1164c09870db76f2aa9133CAS |
Stuefer JF, Huber H (1998) Differential effects of light quantity and spectral light quality on growth, morphology and development of two stoloniferous Potentilla species. Oecologia 117, 1–8.
| Differential effects of light quantity and spectral light quality on growth, morphology and development of two stoloniferous Potentilla species.Crossref | GoogleScholarGoogle Scholar |
Trudgill DL, Honek A, Li D, Van Straalen NM (2005) Thermal time – concepts and utility. Annals of Applied Biology 146, 1–14.
| Thermal time – concepts and utility.Crossref | GoogleScholarGoogle Scholar |
Turc O, Lecoeur J (1997) Leaf primordium initiation and expanded leaf production are co-ordinated through similar response to air temperature in pea (Pisum sativum L.). Annals of Botany 80, 265–273.
| Leaf primordium initiation and expanded leaf production are co-ordinated through similar response to air temperature in pea (Pisum sativum L.).Crossref | GoogleScholarGoogle Scholar |
Turgeon R (1989) The sink-source transition in leaves. Annual Review of Plant Physiology and Plant Molecular Biology 40, 119–138.
| The sink-source transition in leaves.Crossref | GoogleScholarGoogle Scholar |
Valladares F, Niinemets Ü (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology Evolution and Systematics 39, 237–257.
| Shade tolerance, a key plant feature of complex nature and consequences.Crossref | GoogleScholarGoogle Scholar |
Yoshida S, Mandel T, Kuhlemeier C (2011) Stem cell activation by light guides plant organogenesis. Genes & Development 25, 1439–1450.
| Stem cell activation by light guides plant organogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptlSjsbg%3D&md5=d306c7fae78d8d18d99f0ba70672392aCAS |
